The phylum Dinoflagellata encompasses a large diversity of unicellular eukaryotic organisms, including phototrophic taxa, hence playing a major role in the biological pump (Falkowski, 2012). Dinoflagellates are currently found in all aquatic systems, mostly in marine waters, where at least 2377 species are known (Gómez, 2012a). They occur from high latitudes to the tropics and can be found even in sea ice (e.g., Mudie, 1992; Montresor et al., 2003). Some of them are known to create Harmful Algal Blooms (HABs) (i.e., Alexandrium, Dinophysis, Karenia species, etc.).

Dinoflagellates have a complex feeding strategy. Among them, several species are phototrophic and account for an important part of the primary productivity of the ocean together with haptophytes and diatoms (e.g., Sigman and Hain, 2012). However, about 58% of extant taxa are heterotrophic, and several are described as mixotrophs, symbionts or parasites (Gómez, 2012b). One of the striking features of this group is that about 20% of the species form cysts that protect hypnozygote during their life cycle and the cyst is made of highly resistant organic matter enabling preservation in the sediments (e.g., Head, 1996) (Figure 1). These cysts are recovered in palynological slides after chemical treatments involving hydrochloric and hydrofluoric acids, and they are commonly analysed by palynologists as other organic-resistant microfossils such as pollen and spores (Traverse, 1974).

Close to a hundred organic-walled dinoflagellate cyst (also called dinocyst) taxa have been described from recent sediments (Van Nieuwenhove et al., 2020a; Limoges et al., 2020; Mertens et al., 2020). In addition, 35 known extant marine taxa make a calcareous cyst that can also be found in marine sediments (Zonneveld et al., 2005).

Dinoflagellate cysts have been observed in sedimentary rocks dating since the Triassic and used with success as biostratigraphic markers in Mesozoic and Cenozoic sequences (e.g., Fensome et al., 1993). In the 1970s, their significance as a palaeoceanographical indicator emerged with the pioneering studies of Williams (1971), Davey and Rogers (1975), Wall et al. (1977) and Williams and Bujak (1977) dealing with deep-sea sediment of the Atlantic Ocean. Earlier on, the ground-breaking studies of Braarud (1945) and later on of Nordii (1951), Wall (1965) and Wall and Dale (1966) elucidated the relationship between the motile form found in surface waters and the cyst, settled in the sediments, helping to understand the ecological affinities of these organisms. Since then, numerous studies focused both on culture and rDNA sequencing have further increased our knowledge of this relationship (e.g., Wang et al., 2019; Gu et al., 2021, 2022), clarifying taxonomical conundrums.

In the last thirty years, the use of dinoflagellate cyst assemblages in palaeoecology and palaeoclimatology increased considerably, notably with the development of approaches allowing quantitative estimates of past climate and ocean parameters. Here, we present the state of the knowledge concerning dinoflagellate cysts and their ecology, we provide some insight into the use of assemblages to document palaeoceanographical changes in the Atlantic Ocean during cold and warm episodes of the late Quaternary, and we briefly outline some environmental issues involving dinoflagellates and their cysts. Furthermore, this review integrates up-to-date considerations on the distribution of dinocysts both in time (biostratigraphy and ecostratigraphy) and space, from the high latitudes of the Northern Hemisphere to the Southern Ocean, following a major update of the taxonomy (Van Nieuwenhove et al., 2020b).

The life cycle of dinoflagellate is complex, with a hiatus between the thecal stage of living populations and the cyst stage, related to sexual reproduction, that fossilises in the sediment. Whereas thousands of living species are known, less than a hundred recent dinoflagellate cyst taxa were described. Hence, the cyst record only provides a fragmentary picture of the original populations. Furthermore, the morphology of the cyst is distinct from that of the theca, which makes cyst identification one of the most challenging aspects of the analysis. This is particularly critical for some taxa that exhibit a large range of morphological variability. The Spiniferites species are a typical example with shapes showing large variations (e.g., de Vernal et al., 2018; Mudie et al., 2018; Gu et al., 2021). The cyst morphology is the basis for the identification. The shape and the tabulation of the cyst body, the shape and position of the archeopyle, the ornamentation, processes density, shape and position, the wall structure, and sometimes the colour of the wall are all typical characteristics used to identify species. Several comprehensive atlases have been produced over the last decades, illustrating most of the modern dinoflagellate cyst species (e.g., Rochon et al., 1999; Zonneveld et al., 2013; Zonneveld and Pospelova, 2015; Mudie et al., 2017; Limoges et al., 2018, 2020; Mertens et al., 2020; Van Nieuwenhove et al., 2020a).

Another layer of complexity in the study of fossil dinoflagellate cysts is related to the dual terminology used to identify dinoflagellates and their cysts that are observed in distinct types of samples (it follows the International Code for the Nomenclature of Algae, Fungi and Plants (the Shenzhen Code, Turland et al., 2018). On the one hand, we have biological names for the thecate stage, and on the other hand, we have micropalaeontological names for the cyst stage yielding fossils (see Head, 1996; Ellegaard et al., 2018; Head et al., 2024). Although it has not been officially agreed, in general, studies dealing with cysts use the micropalaeontological name, unless the cyst was originally described from specimens of known biological affinity (see Table 1).

The wall of organic-walled dinoflagellate cysts is made of a strong molecules, often called dinosporin although recent studies have shown complex compositions depending upon the taxa. Studies based on micro-Fourier-transformed infrared spectroscopy have highlighted distinct compositions whether the taxon is phototrophic (cellulose-like glucan) or heterotrophic (nitrogen-rich glucan) (e.g., Bogus et al., 2014; Gurdebeke et al., 2018, 2020; Meyvisch et al., 2022, 2023). Some studies on the preservation aspect of organic matter in oxic and anoxic environments have tentatively established a classification of taxa according to a sensitivity gradient, with most phototrophic species being relatively resistant whereas heterotrophic species would be more prone to early diagenetic processes (e.g., Zonneveld et al., 2008, 2019; Versteegh and Zonneveld, 2022).

The complexity of the life cycle of dinoflagellates and the fact that the production of cysts is still not fully understood, as most of the observations are based on controlled conditions in laboratories (e.g., Bravo and Figueroa, 2014), has long been a limitation in palaeoecology. Consequently, the establishment of dinoflagellate cysts as a palaeoecological indicator slowly evolved, and from studies on the distribution of these microfossils in recent sediments (e.g., Wall et al., 1977; Williams and Bujak, 1977; Harland, 1983; Turon, 1984; Rochon et al., 1999). Mapping their occurrence in the oceans and relating their relative abundance with surface conditions was the stepping-stone to enable this microfossil group to become a valuable tracer of sea-surface conditions (e.g., Rochon et al., 1999; de Vernal et al., 2001; Marret and Zonneveld, 2003; Zonneveld et al., 2013; de Vernal et al., 2020).

Overall, the increasing number of studies investigating the distribution of dinoflagellate cyst species in recent sediments (Figure 2) has greatly contributed to refining our knowledge of their ecological affinity, sometimes shifting paradigms for some species. In parallel, progress in culture techniques and genetic studies has enabled to clarification of the idea that some thecate species may “create” different cyst species likely related to environmental conditions (the Spinifera complex, e.g., Ellegaard et al., 2018). Although there are taxonomical uncertainties and despite the hiatus between living and fossil populations, dinoflagellate cysts are now considered very useful palaeoceanographical tracers in marine environments of continental margins.

Until the 1970s, most studies dealing with fossil dinoflagellate cysts, then designated as hystrichospheres, were undertaken by sedimentary geologists to document the Mesozoic-Cenozoic biostratigraphy. The demonstration of the relationships between dinoflagellates and their cysts based on detailed morphological observations of fossils (Evitt, 1963), observation of hystrichospheres in the plankton (Wall, 1965) and culture experiments (Wall and Dale, 1966, 1968) were an important step toward the use of dinoflagellate cysts in palaeoecology. Based on dinoflagellate cyst taxa counts in 35 surface sediment samples from the North Atlantic Ocean, Williams (1971) demonstrated a distribution related to environmental gradients, from nearshore to offshore settings and with latitudes. Later, Wall et al. (1977) made a comprehensive analysis of the distribution of dinoflagellate cysts in sediments collected at 168 sites from tropical to temperate latitudes of the Atlantic Ocean showing further distinct associations related to the latitudinal gradients, in addition to assemblages having affinities for either estuarine, neritic or oceanic environments. Hence, they proposed an ecological classification of taxa in categories and associations, which could be used as a conceptual model for the understanding of taxa distribution (Figure 3).

Since the early works of Williams (1971) and Wall et al. (1977), regional studies permitted to develop distribution maps of dinoflagellate cysts in sediments of the North Atlantic and adjacent seas (e.g., Harland, 1983; Turon, 1984; de Vernal et al., 1994; Rochon et al., 1999), the Northern Hemisphere Oceans (Radi and de Vernal, 2008; de Vernal et al., 2013a, 2020) and at World Ocean scale (Marret and Zonneveld, 2003; Zonneveld et al., 2013; Marret et al., 2020; see Figure 2). Hence, much progress in the knowledge of the distribution of dinoflagellate cysts in surface sediments has been made in the last decades, strengthening the early observation and inferences by Wall et al. (1977).

Dinoflagellate cysts recovered in sediment are related to pelagic productivity but the taphonomic processes between the dinoflagellate population in upper water mass and their cysts in the thanatocoenoses have been a matter of debate. Comparison of dinoflagellate in plankton tows (theca) and sediment traps or sediments at the sea floor (cysts) have shown a general agreement in the taxonomic content allowing inferences about dinoflagellate populations in surface water and cyst assemblages in the sediment (e.g., Dodge and Harland, 1991; Dodge, 1994; Heikkilä et al., 2016) although only a small proportion of dinoflagellate taxa produces fossilisable cysts (e.g., Head, 1996). While a large part of the cyst fluxes is likely to derive from the upper water masses through settling with marine snow and faecal pellets (Turner, 2015), hydrodynamical factors can be involved in the sedimentation of the cysts (Wall et al., 1977; Nooteboom et al., 2020). Hence, lateral transport of dinoflagellate cysts before burial as any other small-size particles cannot be ruled out. Nevertheless, the sharp boundaries in the cyst distribution on the sea floor suggest a limited impact of distal transport on the assemblages (e.g., de Vernal et al., 2020), as also shown at the zonal scale through modelling experiment (Thöle et al., 2023). The analyses of other microfossils recovered in palynological slides such as pollen and spores that are necessarily allochthonous provide clues about potential nearshore-offshore transport, which appears very limited beyond the estuarine and inner neritic zone (e.g., de Vernal and Giroux, 1991; Rochon and de Vernal, 1994). Among taphonomical processes, selective preservation could be considered. It has been shown that the organic-walled cysts of some taxa, notably those belonging to protoperidinales, could be affected by oxidation (Zonneveld et al., 2008, 2019). Nevertheless, despite possible biases due to differential preservation, the analysis of cyst distribution in recent sediments highlights close relationships with sea-surface conditions (e.g., de Vernal et al., 2020). Abundant protoperidiniale cysts recovered in the sediment may also suggest a limited impact of oxidation, at least along continental margins where productivity is high and sedimentary inputs result in rapid burial.

In general, the concentrations of organic-walled dinoflagellate cysts are high in neritic marine environments and decrease offshore, showing very little fluxes in the distal deep ocean settings (Figure 4A). Such a feature may be due to generally low dinoflagellate productivity in central parts of the ocean, but also to poor preservation or both. Hence, dinoflagellate cysts appear particularly useful for the study of continental margin areas, where their species diversity and abundance are high (Figure 4B).

The modern distribution of dinoflagellate cysts around the world documents the geographical range and ecological affinities of the species. Many taxa can be considered cosmopolitan, meaning they occur in most of the oceans and seas, while others have a more restricted spatial distribution (e.g., Marret et al., 2020). Table 1 highlights that most taxa are found in the three oceans, but their relative abundance can vary in importance. Among the 83 taxa that we discuss here, very few are strictly endemic, and these are mostly found in the Southern Ocean, close to the Antarctic continent (Figure 5). Although McMinn (1995) initially reported the absence of Quaternary dinoflagellate cysts south of 60°S, subsequent studies highlighted a relatively the occurrence of up to 15 taxa, including the new species Cryodinium meridianum, Nucicla umbiliphora, and Selenopemphix antarctica (Marret and de Vernal, 1997; Esper and Zonneveld, 2002; Hartman et al., 2019). Another spot of endemism well documented is the Black Sea-Caspian Sea region, with some species being a legacy from the Paratethyan Sea (e.g., Mudie et al., 2018). It can be noted that recent human activities have enabled the spread of some endemic species. One example is that of Peridinium ponticum, an endemic species from the Ponto-Caspian region abundant in the northwestern part of the Black Sea (Mudie et al., 2017), but recently reported to occur in the Ria de Vigo (Atlantic margin of NW Iberia; García-Moreiras et al., 2023) and off Brittany (Mudie et al., 2017). In these cases, ballast waters, which are rich in micro-organisms that can relocate and thrive in different geographical regions (e.g., Cheniti et al., 2018), may have constituted an efficient mechanism for cyst dispersal.

Among sea-surface conditions that we reconstruct from biogeochemical proxies and microfossil assemblages, palaeoproductivity may be the most challenging one, besides sea-ice cover. Dinocysts have proved to be good indicators of palaeoproductivity, in particular in regions where net primary productivity is possibly the most dominant control on dinoflagellates (see Radi and de Vernal, 2008; Penaud et al., 2018). Coastal regions, where important river discharges (or plumes) occur, are usually characterized by rich dinocyst assemblages, with a zonation linked to the presence of nutrients and hydrographic conditions. The Atlantic Ocean contains zones where Chlorophyll-a (reflecting the abundance of phytoplankton) is highly abundant, mostly along coastal regions where eastern boundary currents occur (Figure 12A). The West African coastline has several sectors with permanent upwelling systems (Canary Current, Benguela Current). The equatorial region has also upwellings linked to the latitudinal movement of the Intertropical Convergence Zone (ITCZ). In the eastern equatorial Atlantic Ocean, major rivers (Congo, Niger) bring in the marine environment freshwater and nutrients, affecting coastal waters up to a certain distance from the shore. The Congo River discharge is known to create the phenomenon of river-induced upwelling, bringing up to the surface nutrients (e.g., Cadée, 1978; Eisma and Van Bennekom, 1978).

A regional database of dinoflagellate cyst assemblages was reviewed in Hardy et al. (2018), evaluating their potential to reconstruct sea-surface conditions, in particular past productivity. Of the 237 sites that were selected, 164 were retained as they could be related to pre-industrial conditions for productivity (using Vertically Generalised Production Model, VGPM) and SST. In this study, two NPP models were used, the VGPM and the Eppley-VGPM ones, where the Eppley-VGPM tends to give higher NPP values when SSTs are high. The statistical analysis (CCA) performed on these 164 assemblages (Figure 12B) shows a clustering of assemblages that more or less identifies the different regimes of oceanographical conditions. A canonical correspondence analysis carried out on the taxa occurring in the 164 assemblages shows that taxa are ordinated along three dominant directions (Figure 12C), which strongly suggests that the species are predominantly controlled by SST and productivity, even though the two NPP vectors have a different direction. Taxa in the upper right quarter are usually found in open ocean and western boundary current systems. Taxa in the bottom left quarter usually respond to warmer temperatures compared to the taxa in the bottom right quarter. Most of the heterotrophic taxa are ordinated closely to both NPP vectors.

This situation is similar back in time. Despite rare organic-walled dinoflagellate cyst records in this region, contrasting data highlight the complex response of dinoflagellate cysts to environmental changes. Selected records covering the last 25,000 years, with robust age models, show that the eastern side of the tropical Atlantic Ocean was mostly dominated by heterotrophic taxa, notably Brigantedinium spp., during the last glaciation, and that the Holocene is characterised by a dominance of phototrophic taxa, mainly O. centrocarpum and some Spiniferites species (Figure 13). Heterotrophic taxa also captured the latitudinal migration of the ITCZ, in particular near the deltas of large rivers (e.g., Marret et al., 2013; Hardy et al., 2018). In the western side of the tropical Atlantic Ocean, the records show the dominance of phototrophic taxa, essentially O. centrocarpum, with very little change between glacial and interglacial conditions.

Further south, very few Quaternary records are available, but they all show a dominance of heterotrophic taxa during glacial marine isotopic stages, notably the MIS2; they also have demonstrated strong potential to trace latitudinal movements of the different fronts (e.g., Esper and Zonneveld, 2007). Off the southwest African coast, ODP Site 1087 integrates signal of Agulhas leakages over the last 500,000 years based on biogeochemical and microfossil proxies; dinoflagellate cysts were used to reconstruct sea-surface temperature, showing a good agreement with alkenone-based SSTs (Petrick et al., 2015). These few studies provide evidence that dinoflagellate cysts can be used to reconstruct complex oceanographic changes over the Quaternary.

Some dinoflagellates are notoriously known for lethal toxin production (e.g., Alexandrium sp.); others are red-tide producers, and while not being lethal, can severely affect aquatic ecosystems through the process of eutrophication (e.g., Anderson, 2019). Global monitoring shows that most coastal regions are now affected by HABs (either red tide or toxicity, or both) (https://data.hais.ioc-unesco.org/); that was not the case half a century ago where fewer events were reported or recorded. Causes of such widespread phenomenon are, among others, related to increased agricultural activities, with the release of nutrients (N and P), favouring algal blooms. Transport of organisms in ship ballast waters has also been a contributor. Recent studies have been linking changes in climatic conditions to phytoplankton communities (e.g., Hinners et al., 2019). Therefore, it was very tempting to trace back in time the occurrence of species related to eutrophication to better understand the mechanisms behind their distribution. The Gulf of Mexico is an exemplary case study where the clear relationship between the abundance of specific cyst taxa (mostly heterotrophic species) and nutrient enrichments due to the use of agricultural fertiliser has been established (Price et al., 2018). Of the known species producing toxins or red-tides, very few produce a cyst that can preserve well in sediments (see Table 1, thecate species in bold). Cysts of Alexandrium sp. are often observed in recent sediments and up to a few hundred years but do not seem to be preserved beyond that (e.g., Head et al., 2006). It was debated that these cysts may have been confused with the ones produced by the calcareous dinoflagellate species, Scrippsiella trifida. Mudie et al. (2002) reported sporadic presence of Alexandrium cysts off Newfoundland during the Holocene period, their abundance linked to warming SST. However, Head et al. (2006) demonstrated that these cysts were produced by S. trifida. Nevertheless, other species, which produced resistant cysts, have shown high abundance during warm episodes (L. machaerophorum during the Holocene in the NW Atlantic Ocean, Mudie et al. (2002); Polysphaeridium zoharyi during the Middle Eocene Climatic Optimum warming in east equatorial Atlantic, Cramwinckel et al., 2019).

Fjords have been particularly scrutinised, due to their propensity of becoming eutrophic in recent times. Dale et al. (1999) introduced the concept of using abundance of dinoflagellate cysts as “indicators of cultural eutrophication”. L. machaerophorum, a species occurring worldwide, with a large tolerance to salinity and temperature, has seen their abundance largely increase when additional nutrients entered the waters of the inner basin of the studied fjord (Oslofjord, Norway). Not far from this site, another record from Gullmar Fjord (Sweden) highlights a more complex story, with no strong evidence of the abundance of L. machaerophorum being related to nutrient enrichments (Harland et al., 2006).

Our increasing knowledge of the ecology of dinoflagellate cyst species and their biogeographical distribution highlights that their past occurrence reflects a complex history of oceanographic changes, in particular for more recent times where human activities had a profound impact on coastal ecosystems. However, it is possible to use past assemblages during interglacial periods to obtain an insight into environmental conditions in a warmer world.

Compared to other microfossils, dinoflagellate cysts are very particular palaeoecological-palaeoceanographical indicators as summarized in a few points below.

For all the reasons mentioned above, dinoflagellate cyst assemblages are unique proxies allowing the documenting of past climate and ocean conditions with regard not only to temperature but also considering seasonality, salinity, sea-ice cover, and productivity. However, the taxonomy of dinoflagellate cysts is not necessarily easy, especially when considering the polymorphism of some taxa and the existence of cryptic species. Moreover, the processing of the sediment before microscope observation and the analyses of the dinoflagellate cyst population are time-consuming. As a consequence, the scientific community is currently exploring techniques such as those based on molecular biomarkers and ancient DNA that are less tedious than micropalaeontology to document past dinoflagellate populations and/or species as proxies for key environmental parameters.

FM: Conceptualization, Writing – original draft, Writing – review & editing. AV: Conceptualization, Writing – original draft, Writing – review & editing.